Ciência1510 Rural, Santa Maria, v.37, n.6, p.1510-1517, nov-dez, 2007 Bueno et al. ISSN 0103-8478

Serpentine leafminer ( trifolii) on (Solanum tuberosum): field observations and plant photosynthetic responses to injury

Mosca-minadora () na cultura da batata (Solanum tuberosum): observações de campo e respostas fotossintéticas da planta à injúria

Adeney de Freitas BuenoI Benjamin ZechmannII William Wyatt HobackII Regiane Cristina Oliveira de Freitas BuenoIII Odair Aparecido FernandesIV

ABSTRACT da batata. Recentemente, a mosca-minadora (Liriomyza trifolii) tem tornado-se uma praga importante na cultura da batata. Serpentine leafminers, Liriomyza spp. (Diptera: As larvas comem o mesófilo foliar, deixando longas minas no ), are polyphagous that feed on numerous interior das folhas. O efeito na fotossíntese do tecido foliar crops worldwide including potato. Recently, leafminer larvae remanescente das minas é desconhecido. Em 2003, as respostas (Liriomyza trifolii) have become an economically important fisiológicas das plantas de batata à mosca-minadora L. trifolii pest of potato. The larvae eat the mesophyll of leaflets leaving foram avaliadas no condato de Kearney, Nebraska, EUA. As long winding tunnels inside the leaflets. The photosynthetic avaliações de área foliar danificada, fotossíntese e fluorescência effects of larval tunneling on the remaining leaf tissue are foram feitas aos 7 e 14 dias após a infestação. A moscas- unknown. In 2003, physiological responses of potato to minadoras causaram até 13% de área foliar danificada, com leafminer, L. trifolii were evaluated in Kearney, Nebraska, USA. nenhuma redução na capacidade fotossintética da área The leaflets were examined 7 and 14 days post infestation for remanescente dos folíolos, tendo, portanto, efeitos semelhantes leaf area injury, photosynthetic rates and fluorescence. aos do grupo dos insetos desfolhadores. Entretanto, os Leafminers caused up to 13% leaf area loss due to leafminer resultados de fluorescência revelaram mudanças na eficiência injury with no effect on the photosynthetic rates of the remaining fotossintética e, dependendo do tipo de injúria, esta pode levar leaf tissue thus having similar effects as other gross tissue a uma senescência precoce da folha. Monitoramentos de campo removers. However, fluorescence measures revealed changes mostraram que o abamectin é eficiente no controle da mosca- in the photosynthetic efficiency and depend of the type of injury, minadora, L. trifolii, com um baixo impacto aos parasitóides it may lead to early leaf senescence. Field monitoring of L. da família Eulophidae, podendo ser uma boa opção de controle trifolii infestations showed that treatments with abamectin were químico. effective in reducing leafminer numbers and had no immediate effect on beneficial parasitoid from Eulophidae family Palavras-chave: interação inseto-planta, controle químico, suggesting that abamectin is a good option for chemical control. fotossíntese.

Key words: plant- interaction, chemical control, photosynthesis INTRODUCTION RESUMO Serpentine leafminers, Liriomyza spp. Moscas-minadoras, Liriomyza spp. (Diptera: Agromyzidae), são pragas polífagas distribuídas por todo o (Diptera: Agromyzidae), are polyphagous worldwide mundo, que se alimentam de diferentes culturas, incluindo a insects that feed on various crops including potato

IDepartamento de Biologia, Universidade de São Paulo (USP), 14040-901, Ribeirão Preto, SP, Brasil. Endereço para correspondência: Condomínio Monte Verde Casa, 156. Rua Dona Firmina s/n, Setor Sítio Recreio dos Ipês, 74681-450, Goiânia, GO, Brasil. E-mail: [email protected]. IIDepartment of Biology, University of Nebraska-Kearney, Kearney NE, 68849, USA. IIIDepartamento de Entomologia, Fitopatologia e Zoologia Agrícola, Universidade de São Paulo (ESALQ/USP), Piracicaba, SP, 13418-900, Brasil. IVDepartamento de Fitossanidade, UNESP, Jaboticabal, SP, Brasil.

Received 04.24.06 Approved 03.21.07 Ciência Rural, v.37, n.6, nov-dez, 2007. Serpentne leafminer (Liriomyza trifolii) on potato (Solanum tuberosum):... 1511

(PARRELLA, 1987). Among the host plants, MATERIAL AND METHODS is one of the most important families (SOUZA, 1993). On potato (Solanum tuberosum), Leafminers: pupae of Liriomyza trifolii were serpentine leafminers were of secondary importance; obtained from a colony maintained at the University of however, biological control agents have been reduced California, Riverside, California, USA. The pupae that by pesticides applied on potato fields, leading to were close to adult emergence were used to infest the leafminer outbreaks of economic importance (EWELL experimental plants. et al., 1990). In Nebraska, USA, L. trifolii outbreaks Field experiment: during August, 2003, two have occurred late in the season during 2003-2005. High field experiments were conducted in a commercial potato levels of infestation (more than 70% of potato leaflets field in Kearney County in south-central Nebraska, infested with at least one leaf miner) have occurred USA using a Frito Lay proprietary chipping variety. and growers have attempted chemical control. In Brazil, Potatoes were planted spaced 0.9 meter between rows leafminers have also being a serious problem for potato having 4 plants/linear meter in each row. In August, growers (SOUZA & REIS, 1999). Therefore, studies to potatoes were in the bulking stage (after blooming). assess plant-leafminer interactions in potato and other Both experiments were conducted using a randomized crops are needed in order to improve economic complete block design, with 8 replicates. The treatments agricultural decision to be made in both North and South were a factorial of 2 (7 and 14 days after infestation) x 3 America. (uncaged control leaflet, caged control leaflet, and The capacity of leafminers to reduce yield infested leaflets) for photosynthetic capacity. has been documented for several crops (SPENCER, Fluorescence measurements were made using a factorial 1973; HILJE et al., 1993). The injury is primarily caused of 2 (7 and 14 days after infestation) x 2 (caged control by the larvae because they start to feed immediately leaflet and infested leaflet). after eclosion and feed constantly until pupation Experimental plants were infested with 10 outside the leaf (PARRELLA, 1987; SOUZA & REIS, pupae of L. trifolii per leaflet by placing pupae in fine- 1999). Liriomyza spp. injury is known to reduce meshed leaf cages. Leafminer injury and control photosynthetic capacity for Chrysanthemum, treatments were imposed on the top central leaflet (Alpium graveolens), (Lycopersicon located on the upper 4th node. Caged control treatment esculentum), and lima (Phaseolus lunatus) (non-infested leaflets) was treated similarly. Seven or (JOHNSON et al., 1983; PARRELLA et al., 1985; 14 days after infestation, cages were removed, TRUMBLE et al., 1985; MARTENS & TRUMBLE, photosynthesis and fluorescence readings were taken 1987). At present, however, the relationship between (see below) and injury was evaluated. L. trifolii mining injury and their effects on potato leaflet Photosynthetic rates (A) and chlorophyll photosynthesis has not been tested. parameters were measured from the same leaflets. All Better knowledge of the plant’s physiological capacity to withstand insect injury and readings were taken on remaining uninjured tissue. The the effect of pesticides on a pest and its natural enemies measurements were made using a portable is necessary before establishing accurate density photosynthesis system (model LI-6400, Li-Cor, Lincoln, NE), with CO injector and light source, which allows treatment levels for any crop system (HIGLEY, 2001). It 2 stable CO concentration and light intensity during all is unclear if the tunneling caused by leafminer larval 2 feeding changes the photosynthetic response of the measurements. The settings used were: blue light -2 -1 remaining leaf tissue of potato. If there are no changes source at 1500 mmol m s photosynthetic photon flux -2 in photosynthetic response in the remaining leaf tissue density (PPFD), CO2 concentration at 400mmol CO2 m then the injury caused by leafminer feeding could be s-1 and the relative humidity inside the chamber was characterized as simple defoliation. Further if leafminer kept between 45-55%. Photosynthetic rates were injury can be called defoliation then economic injury measured on 6cm2 of leaf area, the maximum area levels developed for other defoliating insects could measured by LI-6400. After the photosynthetic also be utilized in the management of this pest. measurements, the leaflets were dark-adapted for 20 Therefore, the objectives of this study were: minutes by using dark leaf clips in order to measure the 1) to examine if the injury caused by L. trifolii would chlorophyll fluorescence parameters (Fv/Fm, qN, qP cause differences in photosynthesis and chlorophyll and ETR) using a leaf chamber fluorometer (Model fluorescence parameters on the remaining tissue and Licor-6400-40, Li-Cor, Lincoln, NE). After the 20 minutes 2) to examine the effects of abamectin pesticide on L. of dark adaptation, the leaves were exposed to the weak, trifolii and its natural enemies, in particular, parasitoids modulated beam for determination of Fo. A pulse of from the family Eulophidae. saturated light (150 PAR for 30 seconds) was imposed

Ciência Rural, v.37, n.6, nov-dez, 2007. 1512 Bueno et al.

to obtain Fm. This allows determination of Fv/Fm of spread to other areas of the field and premature leaf dark adapted leaves. The leaves were then exposed to drop was observed in areas of the SW quadrant of the actinic light (1350 PAR) and saturating pulses of light field, even though, damage was inflicted after bloom were imposed in order to obtain the quenching analysis when potato plants are less susceptible to defoliation, (qP and qN) at steady-state fluorescence. Dark more than one month remained prior to harvest. adaptation was used to get fluorescence data from Although the decision to manage the leafminer leaves with cleared plastoquinone pools. Then the population was made by the farmer, no pesticide instrument was able to collect fluorescence data while information for leafminer in potato was available. Thus the photosynthesis apparatus was collecting light and the farm applied different rates of insecticide to the converting the light into usable ATP and NADPH. SW and southeast (SE) quadrants of the field while Mean weather conditions inside trial area during the leaving the north half (N) of the field as an untreated experimental period was temperature of 24.1oC control or check strip. Abamectin (Agrimek, Syngenta) (maximum and minimum temperatures reached 32.7oC was chosen based on its effectiveness on another and 17.4oC, respectively), a relative humidity varying leafminer, . Treatments were from 41 to 73% and a total precipitation of 8.38mm plus made on July 21 and August 4, 2003, at different rates irrigation accordingly to the farm irrigation schedule for each treatment area. The SW quadrant of the field and needs. received 583mL ha-1 of abamectin and the SE quadrant After all the measurements were taken the received 1166mL ha-1. All field observations were potato leaflets were collected and photographed. The continued until August 13, 2003. leaflet images were digitized, and the percent of leaf Data Analysis: photosynthetic and mined by L. trifolii was determined using image fluorescence data were analyzed using PROC MIXED analysis software (Mocha, Jandel Scientific, San Rafael, procedure of the SAS program (SAS INSTITUTE, 2001). CA). Means were separated by Stundet t-test (P = 0.05). Field observations and insecticide efficacy: a second potato field under commercial production RESULTS AND DISCUSSION located approximately 11 km north of Minden, Kearney County, Nebraska had high populations of L. trifolii Leafminer mining produced mean injury present on July 1, 2003. Field scouting revealed that (±SE) of 8.37 ± 1.78% on day 7 after infestation and the greatest concentration of leafminers was present 12.38 ± 1.78% on day 14 after infestation. Factorial in the southwest (SW) quadrant of the field, so analysis showed no interaction between infestation observations were initially confined to this quadrant. and date (of infestation) at 5% of probability. Also, Observations consisted of pulling 40 leaves from the there was no statistical difference on percentage of 4th node of random plants within the study area injury caused by leafminer between days 7 and 14 approximately every other day beginning on July 2, (Table 1). These results indicate that 7 days after 2003. The leaves were examined in the laboratory and infestation leafminer had completed most of its larval the number of live larvae in the tunnels and number of feeding. Leafminer development cycle is positively parasitized larvae were determined. On 20/July/2003, correlated with temperature from egg to pupa requiring 80% of leaflets contained at least one leafminer and the about 10 days and pupation averaging 9 days at farmer decided that treatment was necessary. In temperatures of 25oC (PARRELLA, 1987; NAKANO, addition to the initial observation area, leafminers had 1993). At temperatures above 35oC, larvae suffer high

Table 1 - Factorial analysis results 3x2 (3 treatments x 2 days of evaluation) for photosynthesis capacity using % of injury as co-variable and means (±SE) of injury (%) at 7 and 14 days after infestation.

Ancova Mined leaf area (%) Effect F Pr > F 7 days after infestation 14 days after infestation Infestation 2,70 0,084 - - day 18,03 0,0002 - - Infestation*day 0,01 0,99 - - block 0,93 0,497 - - Injury 0,06 0,815 8.37 ± 1.78 a 12.38 ± 1.78 a

Means followed by the same letter are not statistically different according to Student t - test (P>0.05).

Ciência Rural, v.37, n.6, nov-dez, 2007. Serpentne leafminer (Liriomyza trifolii) on potato (Solanum tuberosum):... 1513 mortality and field temperatures may have prevented and in Chrysanthemum (PARRELLA et al., 1985). additional larval feeding in some cages. Several factors may explain the differences from our Photosynthetic rates did not differ between findings. It has been shown that potato is, in general, infested leaflets and caged controls (Figure 1a), able to withstand high levels of defoliation without showing that for the level of infestation used in the yield reduction, especially after blooming (SHIELDS & experiment, leafminer injury did not alter WYMAN, 1984). For other crops, infestation levels photosynthesis of remaining tissue (uninjured tissue) were generally higher than those observed in our study. of potato leaves. This finding contrasts reports that MORRISON & REEKIE (1995) showed that degree of Liriomyza spp. injury reduced photosynthesis in celery wounding often influences whether or not injury to (TRUMBLE et al., 1985), in tomato (JOHNSON et al., the leaf itself impairs photosynthesis. For the level of 1983), in lima beans (MARTENS & TRUMBLE 1987), injury observed in this trial, leafminer injury caused

Figure 1 - Photosynthesis (A; a), nonvariable fluorescence (Fo; b), efficiency of the capture of excitation energy (Fv/Fm; c), electron transport rate (ETR; d), nonphotochemical fluorescence quenching (qN; e) and photochemical fluorescence quenching (qP; f). Means (±SE) followed by the same letter within figure are not statistically different according to Student t - test (P>0.05). Figures 1a, b, d, e and f had results from 7 and 14 days combined because factorial analysis did not show significance in the interaction day * infestation (caged control or infested).

Ciência Rural, v.37, n.6, nov-dez, 2007. 1514 Bueno et al. only photosynthetic leaf area reduction. This observed early leaf senescence. Furthermore, the observation is important because lack of difference between injured leaves and control found photosynthetic injury allows grouping of leafminer with 14 days after infestation on Fv/Fm is more likely a further the leaf-mass consumer injury guilds as proposed by decrease of Fv/Fm value on control rather than any PETERSON (2001). If leafminers, even at higher change due to infestation, since infestation level did infestation levels, do not reduce photosynthesis of not increase in intensity. remaining leaf tissue, it may be further possible to Another parameter to be evaluated when create multiple species economic thresholds based on assessing photochemical efficiency is the electron remaining leaf area. transport chain (ETR). The ETR represents the apparent Beyond the importance of establishing photosynthetic electron transport rate in μmol photosynthetic response of plants to biotic stress, electrons m-2 s-1 (MACEDO et al., 2003). Our data show increasingly attention has been focused on aspects of that ETR values for the test plants were not affected photoeclectron transport (MACEDO et al., 2003). by leafminer injury (Figure 1d). Nonphotochemical Fluorescence readings indicate the function of light fluorescence (qN) and photochemical fluorescence (qP) harvesting and photoelectron transport, representing quenching coefficients provide information about the an important tool on evaluating plant stress. Our thylakoid membrane that are important to the proper examination of leaf fluorescence in leafminer-injured functioning of the xanthophyll cycle. Our data indicate potato leaflets provides better insights on the no difference between qN and qP values between physiological response of potato plants to leafminer infested and caged control leaflets (Figures 1e and 1f). injury. MACEDO et al. (2003), found an increase in Thus, the level of leafminer injury obtained in this study nonvariable fluorescence (Fo) to indicate that light did not impact the protective xanthophyl cycle. energy is being lost rather than passed through the Overall, our results indicate that leafminer phoelectron transport chain. Our results do not show injury of up to 13% of total leaf area do not impact any difference between Fo values of infested and caged photosynthetic rates of remaining leaf tissue while control leaflets (Figure 1b). This indicates that the fluorescence results suggest that light absorbance may be a limiting factor for photosynthetic efficiency in amount of light absorbed is being successfully leafminer-injured plants. Also, it is important to point transported through the phoelectron chain. out that plant responses to insect injury might vary at A second measure, the Fv/Fm ratio indicates different levels of biological organization (PETERSON how much light energy captured is being used by the & HIGLEY, 1993). Thus, when photosynthesis is not reaction center and propagated through the altered by insect injury at the individual organ (leaf), it photoelectron transport chain. We found that L. trifolii might be altered at the plant level (PETERSON & injury significantly affected Fv/Fm ratio. There was a HIGLEY, 1993). For example, induced leafmining has significant increase in the mean Fv/Fm ratio 0.427± 0.045 been shown to induce early leaf abscission on American (7 days after infestation) to 0.5707± 0.045 (14 days after holly, (Ilex opca), an ornamental plant (KAHN & infestation) on infested leaflets (P<0.05). On day 14 CORNELL, 1989) and transmit viruses on celery and after infestation, the Fv/Fm ratio of infested leaflets squash (ZITTER & TSAI, 1977). These injuries do not ± (0.5707 0.045) also differed from caged control leaflets affect the injured plant organ exclusively, but affect ± (0.3102 0.045) (p<0.01) (Figure 1c). Chlorophyll the entire plant. They can directly or indirectly reduce fluorescence data was taken from 14:00 to 15:00 hours canopy photosynthetic rates. Consequently, additional what probably led to a general low value for Fv/Fm. research on the mechanisms underlying leafminer injury However, as we do have the controls and the insect on potato plants is still needed. injury is based on treatment comparison, our findings Samples, taken before the first application are still very important in order to clarify leafminer of abamectin, show a general increase in the number of photosynthetic impairment. According to our results, live larvae per 40 leaves (Figure 2a). The number of leafminer injury affects the antennal chlorophyll parasitized leafminer larvae also increased and generally complexes, causing the light to be reflected rather than showed one to two day lag response (Figure 2b). After absorbed. This observation indicates that even though the first treatment of abamectin, the number of larvae no photosynthetic reduction was observed, remaining decreased rapidly in the southwest quadrant of the tissue of infested leaflets was stressed. The lack of field (abamectin 583mL ha-1). While there was no photosynthetic reduction found in this study may be sampling in the southeast quadrant before the explained by the relatively short period of time that abamectin treatment, scouting data suggest that it takes injury was present. Periods longer than 14 days might five to seven days for the abamectin to reduce larval cause a reduction on photosynthesis and may explain population numbers. Samples were taken 3 days after

Ciência Rural, v.37, n.6, nov-dez, 2007. Serpentne leafminer (Liriomyza trifolii) on potato (Solanum tuberosum):... 1515

Figure 2 - (a) Number of live larvae and (b) number of parasitized larvae by sampling date per 40 leaves before and after abamectin spraying. the first treatment and, while populations were never Leafminers are naturally parasitized by a as high as the north or southwest quadrants, the number of wasps belonging to the families , southeast quadrant (abamectin 1166mL ha-1) showed a Eulophidae, and Pteromalidae which provide natural substantial decrease in live larvae. The untreated north control. We recorded the number of parasitized larvae, half of the field exhibited a rapid growth in the leafminer later identified as the family Eulophidae, to determine if larvae population (Figure 2a). natural enemies would control the infestation. We

Ciência Rural, v.37, n.6, nov-dez, 2007. 1516 Bueno et al. found that the number of parasitized larvae were always ACKNOWLEDGMENTS lower than the numbers of live larvae in all study areas and in the north half of the field the number of We acknowledge M. P. Parrella from the Department of Entomology, University of California, Riverside parasitized larvae plateaued at about seven parasitized for sending us the pupae. CSS Farms allowed access to the fields. larvae per 40-leaf sample. However, the number of live The grant support for A. F. Bueno was provided by Fulbright larvae sampled per 40-leaf sample increased almost Commission’s Council for International Exchange of Scholars and CAPES, Brazil. Helpful comments on experimental design exponentially in the latter portion of the observation were provided by Leon Higley, Tulio Macedo, and Paul Nabity. period (Figures 2a and b). These data show that parasitic wasps alone cannot effectively control leafminer larvae REFERENCES at this level of infestation. The numbers of live leafminer larvae were EWELL, P.T. et al. Farmer management of potato insects in Peru. Lima: International Potato Center, 1990. 87p. successfully managed in the southwest (abamectin 583mL ha-1) and the southeast (abamectin 1166mL ha-1) HIGLEY, L.G. Yield loss and pest management. In: quadrants, however the number of parasitized larvae PETERSON, R.K.D.; HIGLEY, L.G.. Biotic stress and yield also decreased in both quadrants (Figures 2a and b). loss. Boca Raton; CRC, 2001. Chap.2, p.13-22. While the higher application rate of abamectin HILJE, L. et al. Validacion de umbrales de accion para el combate immediately reduced the number of live larvae compared de Liriomyza huidobrensis en parcelas de papa en Cartago, to the lower application rate of abamectin, by the end Costa Rica. In: ______. 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